After many frustrating appearances for Manchester City, with few goals, he was sold to Championship team Southampton for £500,000 on 5 July 2006.[5] The fee was partly funded by a prize from Coca-Cola won in a competition amongst fans. He made an immediate impact at Southampton, scoring on his debut against Derby County at Pride Park, and scoring an impressive goal against Wolverhampton Wanderers in a 2–0 win at St. Mary's. He scored a total of 11 goals in the 2006–07 season. In 2007–08 he started the season with goals against Burnley and Queens Park Rangers. He made a total of 121 appearances for the club, scoring 25 goals.

At the end of the 2008–09 season, following Southampton's relegation to League One, Wright-Phillips was released from his contract at the club. On 15 July 2009, he signed a two-year deal with Plymouth Argyle of the Championship.[6] After he recovered from a knee injury, Wright-Phillips made his debut for the club on 15 September 2009 against Watford. The knee injury occurred once again, and he was sidelined for another long-term spell. In January 2010, Wright-Phillips made his long awaited return for Argyle in the FA Cup against Newcastle United. He made his first start for the club against Coventry City in March 2010, and scored his first goal for Plymouth against Bristol City on 16 March 2010. On 11 December 2010, Wright-Phillips scored both goals against Exeter City in the Devon derby in a 2–0 Plymouth win, the second marked his 12th of the season.

On 19 February 2013, he joined Brentford on loan until the end of the season.[12] He was man of the match on 13 April 2013 against Portsmouth. He scored two crucial goals and provided the winning assist for Clayton Donaldson. However, it wasn't enough to see Brentford promoted to the Championship.

On 24 July 2013, Wright-Phillips joined the New York Red Bulls.[13][14] Despite joining the club in the latter part of the season Wright-Phillips was a key contributor in helping New York capture its first major title, the MLS Supporters' Shield.

On 23 April 2014, he scored a hat-trick in a 4–0 win against the Houston Dynamo.[15] Wright-Phillips secured his second hat-trick for New York on 10 May during a 5-4 home loss to the Chicago Fire. Of note, he scored the winner in a friendly against his father's team Arsenal[16] and the equaliser against Bayern Munich in the 2014 MLS All-Star Game. Two days after the All-Star game, Red Bulls Sporting Director Andy Roxburgh claimed that Wright-Phillips' scoring exploits were producing international transfer interest in the player.[17] On 23 August 2014, he scored his 19th and 20th goals of the season in a 4-2 win against Montreal Impact surpassing Juan Pablo Ángel's club record for goals scored in a single season.[18] On 20 September 2014, he returned from a short term injury to record his 3rd hat trick of the 2014 MLS season in a 4-1 win over Seattle Sounders FC.[19] On 26 October 2014 Wright-Phillips scored twice to equal the Major League Soccer season goal record of 27 goals as New York beat Sporting Kansas City 2-0 in the league’s regular-season finale.[20] Wright-Phillips again scored twice for the Red Bulls in their first match of the 2014 MLS Cup Playoffs, once again against Sporting Kansas City in a 2-1 victory. He scored his third play-off goal against D.C. United in the first leg of the 2014 MLS Eastern Conference semi-final helping New York to a 2-0 victory.

Following his 2014 success, New York signed Wright-Phillips to a designated player contract for 2015.[21] On 22 March 2015 Wright-Phillips scored his first goal of the season and assisted Lloyd Sam on another in a 2–0 victory over rivalD.C. United at Red Bull Arena earning him MLS Player of the Week honors.[22] The following week Wright-Phillips was selected to the MLS Team of the Week for his performance in a 2-1 victory over Columbus Crew in which he scored his second goal of the season and assisted on Mike Grella's game-winning goal.[23] On 10 May, he scored both goals as the Red Bulls won 2–1 at home against New York City FC in the first match between the two franchises,[24] and equalised in a 3–1 victory at the rivals' Yankee Stadium on 28 June.[25] On 11 July, he helped New York to a 4-1 victory over New England Revolution scoring twice during the match.[26]

On 1 August 2015, Wright-Phillips scored the opening goal for New York in a 3–1 away victory over Philadelphia Union. He was assisted on the goal by his brother Shaun who was making his debut for New York.[27]

Wright-Phillips represented England at U20 level. He was first called up in February 2005 and he made his debut as a half time substitute in a 2-0 friendly victory against Russia.[28] He was called up again that summer for the 2005 Toulon Tournament where he played Tunisia,[29] South Korea[30] and the third-place playoff penalty shootout victory over Mexico. [31]

On 9 March 2008, Wright-Phillips, along with Southampton team-mate Nathan Dyer, was accused of stealing money, mobile phones and other items from bar staff at Bar Bluu in Southsea in the early hours of 28 February 2008. CCTV footage taken at the time appeared to show a theft taking place.[32]

On 25 March 2008, Dyer and Wright-Phillips were both arrested over the theft and were questioned at a Portsmouth police station.[33] They were formally charged with burglary on 17 June. They appeared before Portsmouth magistrates on 8 July 2008.[34] Dyer was convicted of burglary and sentenced to community service and made to pay compensation and costs. Wright-Phillips pleaded not guilty, and opted to be tried at Crown Court. He was due to appear before Portsmouth magistrates again on 2 September 2008.[35] However, the case was dismissed by the District Judge following legal argument from Wright-Phillips' barrister, Rupert Bowers, that there was insufficient evidence.[36]

A year later, he and team-mate David McGoldrick were arrested on suspicion of assaulting a Southampton supporter while on a night out. The 21-year-old fan told police that he was attacked by the two footballers in a Southampton street as he made his way home from a night out. The incident is alleged to have happened on 7 February 2009 after players went drinking in the city.[37] On 13 March, the club announced: "After a thorough police investigation the Crown Prosecution Service has decided not to press any charges against either Bradley Wright-Phillips or David McGoldrick, and no further action will be taken against them."[38]